Deciduous forest responses to temperature, precipitation, and drought imply complex climate change impacts Yingying Xiea,1, Xiaojing Wangb, and John A. Silander Jr.a aDepartment of Ecology and Evolutionary Biology, University of Connecticut, Storrs, CT 06269-3043; and bDepartment of Statistics, University of Connecticut, Storrs, CT 06269-4120 Edited by William H. Schlesinger, Cary Institute of Ecosystem Studies, Millbrook, NY, and approved September 23, 2015 (received for review May 21, 2015) Changes in spring and autumn phenology of temperate plants in to when greenness starts to decrease (i.e., onset of leaf coloration) recent decades have become iconic bio-indicators of rapid climate and dormancy dates occur when greenness reaches a minimum value change. These changes have substantial ecological and economic (brown leaves with leaf drop) (27) (SI Appendix,Figs.S1andS2). impacts. However, autumn phenology remains surprisingly little Currently, most studies consider short day length and low tempera- studied. Although the effects of unfavorable environmental ture as the primary or only external triggers of autumn phenology (28, conditions (e.g., frost, heat, wetness, and drought) on autumn 29). However, over the past 60 y (25, 30, 31), researchers studying the phenology have been observed for over 60 y, how these factors physiology of leaf senescence and dormancy have enumerated a interact to influence autumn phenological events remain poorly range of other environmental conditions that may influence autumn understood. Using remotely sensed phenology data from 2001 to phenology, including frost, moisture conditions, and extreme weather 2012, this study identified and quantified significant effects of a events (e.g., drought- and heat-stress, and flooding). Although the suite of environmental factors on the timing of fall dormancy of effects of a subset of these factors on plant leaf coloration and leaf deciduous forest communities in New England, United States. drop were reported by a handful of physiological experiments (32, Cold, frost, and wet conditions, and high heat-stress tended to 33), few studies have quantified the response of fall phenology to a induce earlier dormancy of deciduous forests, whereas moderate full suite of potential explanatory factors. Ongoing climate changes ECOLOGY heat- and drought-stress delayed dormancy. Deciduous forests in are likely to introduce higher frequency and intensity of climatic stress two eco-regions showed contrasting, nonlinear responses to variation factors (34), so it is important to include these in developing more in these explanatory factors. Based on future climate projection over predictive, mechanistic models of fall phenology. two periods (2041–2050 and 2090–2099), later dormancy dates were To study landscape-scale forest phenology, we used satellite remotely sensed autumn dormancy dates of deciduous forests in predicted in northern areas. However, in coastal areas earlier dormancy New England, United States, from the Moderate Resolution Im- dates were predicted. Our models suggest that besides warming in aging Spectroradiometer (MODIS) data product (27) (SI Appendix, climate change, changes in frost and moisture conditions as well as Fig. S1). Greenness of forest canopy reaches the minimum values at extreme weather events (e.g., drought- and heat-stress, and flooding), the dormancy date (27), a proxy for plant fall dormancy (SI Ap- should also be considered in future predictions of autumn phenology pendix, Figs. S1 and S2). We examined dormancy dates of de- in temperate deciduous forests. This study improves our understanding ciduous forest communities in two eco-regions (NH, Northeastern of how multiple environmental variables interact to affect autumn Highlands; NCZ, Northeastern Coastal Zone) from 2001 to 2012 phenology in temperate deciduous forest ecosystems, and points the (Figs. 1 and 2). Multiple environmental factors affecting fall forest way to building more mechanistic and predictive models. dormancy were identified representing spatially and temporally varying chill and frost-stress, heat-stress, drought-stress, precipitation, Land-surface phenology | dormancy date | frost | New England Significance lant phenological shifts in recent decades are iconic bio-indica- – Ptors of climate change (1 4). These phenological changes in turn Autumnal phenological shifts (leaf senescence and dormancy) be- have cascading ecological effects on species demography, biotic in- – cause of climate change bring substantial impacts on community teractions, and ecosystem functions (5 8). Whereas mechanisms of and ecosystem processes (e.g. altered C and N cycling and phe- spring phenology (i.e., bud burst, leafing out, and flowering) are well – nological mismatches) and the fall foliage ecotourism industry. studied (9 13), fall phenology (i.e., leaf senescence and dormancy, However, the understanding of the environmental control of au- indicated by visual signals from leaf coloration and leaf drop) re- tumn phenology has changed little over the past 60 y. We found – mains little studied (14 16). Changes in timing of autumn phenology that cold, frost, wet, and high heat-stress lead to earlier dormancy play a significant role in growing season length prediction, C and N dates across temperate deciduous forest communities, whereas – cycling, and biotic interactions (8, 17 19). Furthermore, delayed leaf moderate heat- and drought-stress delayed dormancy. Divergent coloration and more muted autumn foliage in response to climate future responses of fall dormancy timing were predicted: later for change will likely significantly affect the multibillion dollar fall foliage northern regions and earlier for southern areas. Our findings im- ecotourism industry (20–22). Although delayed leaf coloration and prove understanding of autumn phenology mechanisms and leaf drop in deciduous forests have been observed across the suggests complex interactions among environmental conditions northern hemisphere in recent decades (14, 23, 24), the full range of affecting autumn phenology now and in the future. environmental triggers and how they influence fall phenological changes now or in the future remain poorly understood. Author contributions: Y.X. and J.A.S. designed research; Y.X. and J.A.S. performed re- Autumn phenology of deciduous woody plant species in temperate search; X.W. contributed new reagents/analytic tools; Y.X. and X.W. analyzed data; Y.X., regions is the timing of the developmental stages of leaf senescence X.W., and J.A.S. wrote the paper. and dormancy. Plant physiologists demark leaf senescence beginning The authors declare no conflict of interest. with onset of leaf coloration, and dormancy with leaf drop and the This article is a PNAS Direct Submission. development of dormant apical meristems (25, 26). As detected by 1To whom correspondence should be addressed. Email: [email protected]. remotely sensed satellite images, autumn phenology dates describe This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. the timing of loss of leaf greenness. Leaf senescence dates correspond 1073/pnas.1509991112/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1509991112 PNAS | November 3, 2015 | vol. 112 | no. 44 | 13585–13590 Downloaded by guest on October 2, 2021 and flooding events (Table 1), as well as latitude (a proxy for pho- showed different sensitivities to environmental variation (Table 2). toperiod) and elevation. We built models independently using eight We found that deciduous forests in the NH were more sensitive to different statistical regression methods [including multiple linear re- changes of latitude (i.e., photoperiod), drought, and summer rain- gression, penalized regression methods, Bayesian model averaging fall than the NCZ forests, whereas deciduous forests in the NCZ (BMA) (35), and Bayesian spike and slab regression (36)] to select were more sensitive to change of elevation, chill-stress, autumn significant environmental drivers of dormancy dates of deciduous rainfall, and heavy rain events (Table 2 and SI Appendix,Fig.S3). forest communities, and to assess spatiotemporal responses of dor- The interaction between summer rain and heat in two models mancy dates to those drivers. By model selection criteria and root suggested that to some extent summer rain reduced the effect of mean square error (RMSE), the best models were selected to predict heat-stress on forest dormancy dates, especially for NCZ forests. future dormancy dates of deciduous forest communities in two 10-y The variables that were unique to each of the two models periods (2040–2050 and 2090–2099) with two greenhouse gas con- indicate that dormancy dates for deciduous forests in two eco- centration scenarios [representative concentration pathway (RCP) regions had different responses to frost, seasonal drought-stress, 4.5 and RCP 8.5] under future climate change projections (37). and seasonal rainfall conditions (Table 2). Dormancy dates of NH deciduous forests were influenced by frost in both spring Results (earlier) and autumn (nonlinear), whereas dormancy dates Statistical regressions between fall dormancy dates and the suite in the NCZ were affected significantly only by autumn frost (ear- of predictor variables showed that a number of environmental/ lier). Moreover, the response of dormancy dates in NCZ forests weather conditions significantly affect dormancy dates. The different to frost was also related to elevation; the significant interac- variable